Synaptic transmission at retinal ribbon synapses

Progress in Retinal and Eye Research

Volumn 24, Issue 6, 2005, Pages 682-720

  Heidelberger, Ruth ^a   Thoreson, Wallace B ^b   Witkovsky, Paul ^c  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL; CANNABINOID; DOPAMINE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; INSULIN; NITRIC OXIDE; POLYUNSATURATED FATTY ACID; PROTON; RETINOID; SOMATOSTATIN; ZINC;

CALCIUM CELL LEVEL; CALCIUM TRANSPORT; EXOCYTOSIS; MEMBRANE POTENTIAL; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA; RETINA BIPOLAR GANGLION CELL; REVIEW; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM CHANNELS; EXOCYTOSIS; NERVE ENDINGS; PHOTORECEPTORS; RETINA; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 24344454662     PISSN: 13509462     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.preteyeres.2005.04.002     Document Type: Review

References (366)

1. T. Akagi, M. Kaneda, K. Ishii, and T. Hashikawa Differential subcellular localization of zinc in the rat retina J. Histochem. Cytochem. 49 2001 87 96
2. A. Akopian, D. Krizaj, and P. Witkovsky Contribution of two voltage-dependent calcium currents to the light-evoked responses of retinal horizontal cells Brain Res. 762 1997 121 130
3. 2+ currents in rod and cone photoreceptors of the salamander retina J. Neurosci. 20 2000 929 936
4. B.A. Allwardt, A.B. Lall, S.E. Brockerhoff, and J.E. Dowling Synapse formation is arrested in retinal photoreceptors of the zebrafish nrc mutant J. Neurosci. 21 2001 2330 2342
5. G. Alvarez de Toledo, and J.M. Fernandez Compound versus multigranular exocytosis in peritoneal mast cells J. Gen. Physiol. 95 1990 397 409
6. S. An, and D. Zenisek Regulation of exocytosis in neurons and neuroendocrine cells Curr. Opin. Neurobiol. 14 2004 522 530
7. J.F. Ashmore, and D.R. Copenhagen An analysis of transmission from cones to hyperpolarizing bipolar cells in the retina of the turtle J. Physiol. (Lond.) 340 1983 569 597
8. D. Attwell, S. Borges, S.M. Wu, and M. Wilson Signal clipping by the rod output synapse Nature 328 1987 522 524
9. G.J. Augustine How does calcium trigger neurotransmitter release? Curr. Opin. Neurobiol. 11 2001 320 326
10. G.J. Augustine, E.M. Adler, and M.P. Charlton The calcium signal for transmitter secretion from presynaptic nerve terminals Ann. NY Acad. Sci. 635 1991 365 381
11. G.B. Awatramani, and M.M. Slaughter Origin of transient and sustained responses in ganglion cells of the retina J. Neurosci. 20 2000 7087 7095
12. C.R. Bader, D. Bertrand, and E.A. Schwartz Voltage-activated and calcium-activated currents studied in rod inner segments from the salamander retina J. Physiol. (Lond.) 331 1982 253 284
13. S.L. Ball, P.A. Powers, H-S. Shin, C.W. Morgans, N.S. Peachey, and R.G. Gregg Role of the β2 subunit of voltage-dependent calcium channels in the retinal outer plexiform layer Invest. Ophthalmol. Vis. Sci. 43 2002 1595 1603
14. B. Barbour, B.U. Keller, I. Llano, and A. Marty Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells Neuron 12 1994 1331 1343
15. S. Barnes, and Q. Bui Modulation of calcium-activated chloride current via pH-induced changes of calcium channel properties in cone photoreceptors J. Neurosci. 11 1991 4015 4023
16. S. Barnes, and B. Hille Ionic channels of the inner segment of tiger salamander cone photoreceptors J. Gen. Physiol. 94 1989 719 743
17. S. Barnes, and M.E.M. Kelly Calcium channels at the photoreceptor synapse Adv. Exp. Med. Biol. 514 2002 465 476
18. S. Barnes, V. Merchant, and F. Mahmud Modulation of transmission gain by protons at the photoreceptor output synapse Proc. Natl. Acad. Sci. USA 90 1993 10081 10085
19. 2+ channel Cav1.4α1 from mouse retina Invest. Ophthalmol. Vis. Sci. 45 2004 708 713
20. D.A. Baylor, M.G. Fuortes, and P.M. O'Bryan Receptive fields of cones in the retina of the turtle J. Physiol. (Lond.) 214 1971 265 294
21. N.T. Bech-Hansen, M.J. Naylor, T.A. Maybaum, W.G. Pearce, B. Koop, G.A. Fishman, M. Mets, M.A. Musarella, and K.M. Boycott Loss-of-function mutations in a calcium channel alphal-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness Nat. Genet. 19 1998 264 267
22. J.H. Belgum, and D.R. Copenhagen Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus) J. Physiol. (Lond.) 396 1988 225 245
23. E.E. Bellocchio, R.J. Reimer, R.T. Fremeau Jr., and R.H. Edwards Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter Science 289 2000 957 960
24. A.K. Berntson, and C.W. Morgans Distribution of the presynaptic calcium sensors, synaptotagmin I/II and synaptotagmin III, in the goldfish and rodent retinas J. Vision 3 2003 274 280
25. A. Berntson, and W.R. Taylor The unitary event amplitude of mouse retinal on-cone bipolar cells Vis. Neurosci. 20 2003 621 626
26. A. Berntson, W.R. Taylor, and C.W. Morgans Molecular identity, synaptic localization, and physiology of calcium channels in retinal bipolar cells J. Neurosci. Res. 71 2003 146 151
27. M.J. Berridge Neuronal calcium signaling Neuron 21 1998 13 26
28. D. Bertrand, M.G. Fuortes, and J. Pochobradsky Action of EGTA and high calcium on the cones in the turtle retina J. Physiol. (Lond.) 275 1978 419 437
29. D. Beutner, T. Voets, E. Neher, and T. Moser Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse Neuron 29 2001 681 690
30. C. Blazynski, and M.T. Perez Adenosine in vertebrate retina: localization, receptor characterization, and function Cell Mol. Neurobiol. 11 1991 463 484
31. T.A. Blute, B. Mayer, and W.D. Eldred Immunocytochemical and histochemical localization of nitric oxide synthase in the turtle retina Vis. Neurosci. 14 1997 717 729
32. +-evoked depolarization Brain Res. 482 1989 164 168
33. J.G. Borst, and B. Sakmann Depletion of calcium in the synaptic cleft of a calyx-type synapse in the rat brainstem J. Physiol. (Lond.) 521 1999 123 133
34. J.G. Borst, and B. Sakmann Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem Philos. Trans. R. Soc. Lond. B 354 1999 347 355
35. J.H. Brandstatter, S. Lohrke, C.W. Morgans, and H. Wassle Distributions of two homologous synaptic vesicle proteins, synaptoporin and synaptophysin, in the mammalian retina J. Comp. Neurol. 370 1996 1 10
36. J.H. Brandstatter, H. Wassle, H. Betz, and C.W. Morgans The plasma membrane protein SNAP-25, but not syntaxin, is present at photoreceptor and bipolar cell synapses in the rat retina Eur. J. Neurosci. 8 1996 823 828
37. J.H. Brandstatter, E.L. Fletcher, C.C. Garner, E.K. Gundelfinger, and H. Wassle Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina Eur. J. Neurosci. 11 1999 3683 3693
38. D. Bruns, and R. Jahn Molecular determinants of exocytosis Pflugers Arch. 443 2002 333 338
39. N.E. Buckley, S. Hansson, G. Harta, and E. Mezey Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat Neuroscience 82 1998 1131 1149
40. G.C. Budd, B. Pansky, and L. Glatzer Preproinsulin mRNA in the rat eye Invest. Ophthalmol. Vis. Sci. 34 1993 463 469
41. A.H. Bunt Enzymatic digestion of synaptic ribbons in amphibian retinal photoreceptors Brain Res. 25 1971 571 577
42. P.M. Burger, E. Mehl, P.L. Cameron, P.R. Maycox, M. Baumert, F. Lottspeich, P. De Camilli, and R. Jahn Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate Neuron 3 1989 715 720
43. D.A. Burkhardt Synaptic feedback, depolarization, and color opponency in cone photoreceptors Vis. Neurosci. 10 1993 981 989
44. D.A. Burkhardt, J. Gottesman, and W.B. Thoreson Prolonged depolarization in turtle cones evoked by current injection and stimulation of the receptive field surround J. Physiol. (Lond.) 407 1988 329 348
45. D.A. Burkhardt, S.Q. Zhang, and J. Gottesman Prolonged depolarization in rods in situ Vis. Neurosci. 6 1991 607 614
46. C. Burris, K. Klug, I.T. Ngo, P. Sterling, and S. Schein How Muller glial cells in macaque fovea coat and isolate the synaptic terminals of cone photoreceptors J. Comp. Neurol. 453 2002 100 111
47. L. Cadetti, W.B. Thoreson, and M. Piccolino Pre- and post-synaptic effects of manipulating surface charge with divalent cations at the photoreceptor synapse Neuroscience 129 2004 791 801
48. L. Cao, and W.D. Eldred Subcellular localization of neuronal nitric oxide synthase in turtle retina: electron immunocytochemistry Vis. Neurosci. 18 2001 949 960
49. W.A. Catterall Structure and function of voltage-sensitive ion channels Science 242 1988 50 61
50. 2+ channels Annu. Rev. Cell Dev. Biol. 16 2000 521 555
51. W.A. Catterall, J. Striessnig, T.P. Snutch, and E. Perez-Reyes International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: calcium channels Pharmacol. Rev. 55 2003 579 581
52. O. Cen, M.M. Gorska, S.J. Stafford, S. Sur, and R. Alam Identification of UNC119 as a novel activator of SRC-type tyrosine kinases J. Biol. Chem. 278 2003 8837 8845
53. L. Cervetto, A. Menini, G. Rispoli, and V. Torre The modulation of the ionic selectivity of the light-sensitive current in isolated rods of the tiger salamander J. Physiol. (Lond.) 406 1988 181 198
54. R.L. Chappell, J. Zakevicius, and H. Ripps Zinc modulation of hemichannel currents in Xenopus oocytes Biol. Bull. 205 2003 209 211
55. 2+ channels J. Gen. Physiol. 108 1996 363 374
56. P. Chi, P. Greengard, and T.A. Ryan Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies Neuron 38 2003 69 78
57. P.J. Church, and E.F. Stanley Single L-type calcium channel conductance with physiological levels of calcium in chick ciliary ganglion neurons J. Physiol. (Lond.) 496 1996 59 68
58. J.D. Clements Transmitter time course in the synaptic cleft: its role in central synaptic function Trends Neurosci. 19 1996 163 171
59. D.P. Corey, J.M. Dubinsky, and E.A. Schwartz The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina J. Physiol. (Lond.) 354 1984 557 575
60. R. Cristiani, C. Petrucci, M. Dal Monte, and P. Bagnoli Somatostatin (SRIF) and SRIF receptors in the mouse retina Brain Res. 936 2002 1 14
61. R.A. Cunha, A.M. Sebastiao, and J.A. Ribeiro Ecto-5′-nucleotidase is associated with cholinergic nerve terminals in the hippocampus but not in the cerebral cortex of the rat J. Neurochem. 59 1992 657 666
62. 1 receptors J. Neurosci. 18 1998 1987 1995
63. A. Das, B. Pansky, and G.C. Budd Demonstration of insulin-specific mRNA in cultured rat retinal glial cells Invest. Ophthalmol. Vis. Sci. 28 1987 1800 1810
64. W.W. Dawson, C.F. Jimenez-Antillon, J.M. Perez, and J.A. Zeskind Marijuana and vision - after ten years' use in Costa Rica Invest. Ophthalmol. Vis. Sci. 16 1977 689 699
65. J. del Castillo, and B. Katz Statistical factors involved in neuromuscular facilitation and depression J. Physiol. (Lond.) 124 1954 574 585
66. 2+ current in mammalian cone photoreceptors Neuron 32 2001 1107 1117
67. S.H. De Vries, and E.A. Schwartz Kainate receptors mediate synaptic transmission between cones and 'Off' bipolar cells in a mammalian retina Nature 397 1999 157 160
68. O. Dick, I. Hack, W.D. Altrock, C.C. Garner, E.D. Gundelfiner, and J.H. Brandstatter Localization of the presynaptic cytomatric protein piccolo at ribbon and conventional synapses in the rat retina: comparison with bassoon J. Comp. Neurol. 439 2001 224 234
69. O. Dick, S. tomDieck, W.D. Altrock, J. Ammermuller, R. Weiler, C.C. Garner, E.K. Gundelfinger, and J.H. Brandstatter The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina Neuron 37 2003 775 786
70. I. Dietzel, and U. Heinemann Dynamic variations of the brain cell microenvironment in relation to neuronal hyperactivity Ann. NY Acad. Sci. 481 1986 72 86
71. D.A. DiGregorio, Z. Nusser, and R.A. Silver Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse Neuron 35 2002 521 533
72. M.B.A. Djamgoz, and P.J. Laming Micro-electrode measurements and functional aspects of chloride activity in cyprinide fish retina: extracellular activity and intracellular activities of L- and C-type horizontal cells Vision Res. 27 1987 1481 1489
73. M.B. Djamgoz, R. Aguilo, E.H. Greenstreet, R. Reynolds, and G.P. Wilkin Histochemistry of NADPH-diaphorase - a marker for neuronal nitric oxide synthase - in the carp retina Neurochem. Int. 28 1996 283 291
74. J.E. Dowling The Retina: an Approachable Part of the Brain 1987 Belknap Press Cambridge, MA
75. J.E. Dowling, and F.S. Werblin Organization of the retina of the mudpuppy, Necturus maculosus. I. Synaptic structure J. Neurophysiol. 32 1969 315 338
76. T.V. Dunwiddie, L. Diao, and W.R. Proctor Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus J. Neurosci. 17 1997 7673 7682
77. B.W. Edmonds, F.D. Gregory, and F.E. Schweizer Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells J. Physiol. (Lond.) 560 2004 439 450
78. 2 adenosine receptors in the mammalian brain: evidence for inhibition vs. enhancement of voltage gated calcium channels and neurotransmitter release Prog. Brain Res. 120 1999 265 273
79. S. Eliasof, and F. Werblin Characterization of the glutamate transporter in retinal cones of the tiger salamander J. Neurosci. 13 1993 402 411
80. S. Eliasof, J.L. Arriza, B.H. Leighton, M.P. Kavanaugh, and S.G. Amara Excitatory amino acid transporters of the salamander retina: identification, localization, and function J. Neurosci. 18 1998 698 712
81. K.L. Engisch, and M.C. Nowycky Calcium dependence of large dense-cored vesicle exocytosis evoked by calcium influx in bovine adrenal chromaffin cells J. Neurosci. 16 1996 1359 1369
82. G.J. Evans, and A. Morgan Regulation of the exocytotic machinery by cAMP-dependent protein kinase: implications for presynaptic plasticity Biochem. Soc. Trans. 31 2003 824 827
83. S.-F. Fan, and S. Yazulla Biphasic modulation of voltage-dependent currents of retinal cones by cannabinoid CB1 receptor agonist WIN 55212-2 Vis. Neurosci. 20 2003 177 188
84. S.-F. Fan, and S. Yazulla Inhibitory interaction of cannabinoid CB1 receptor and dopamine D2 receptor agonists on voltage-gated currents of goldfish cones Vis. Neurosci. 21 2004 69 77
85. A. Feigenspan, and R. Weiler Electrophysiological properties of mouse horizontal cell GABAA receptors J. Neurophysiol. 92 2004 2789 2801
86. S.D. Fenster, M.M. Kessels, B. Qualmann, W.J. Chung, J. Nash, E.D. Gundelfinger, and C.C. Garner Interactions between Piccolo and the actin/dynamin-binding protein Abp1 link vesicle endocytosis to presynaptic active zones J. Biol. Chem. 278 2003 20268 20277
87. E.M. Fenwick, A. Marty, and E. Neher Sodium and calcium channels in bovine chromaffin cells J. Physiol. (Lond.) 331 1982 599 635
88. R.D. Fields, and M.H. Ellisman Synaptic morphology and differences in sensitivity Science 228 1985 197 199
89. A.P. Fox, M.C. Nowycky, and R.W. Tsien Single-channel recordings of three types of calcium channels in chick sensory neurones J. Physiol. (Lond.) 394 1987 173 200
90. B.B. Fredholm Modulation of neurotransmitter release by heteroreceptors D.A. Powis S.J. Bunn Neurotransmitter Release and its Modulation 1995 Cambridge University Press New York 104 121
91. M. Frerking, and M. Wilson Saturation of postsynaptic receptors at central synapses? Curr. Opin. Neurobiol. 6 1996 395 403
92. B. Fyk-Kolodziej, P. Qin, A. Dzhagaryan, and R.G. Pourcho Differential cellular and subcellular distribution of glutamate transporters in the cat retina Vis. Neurosci. 21 2004 551 565
93. L. Gaal, B. Roska, S.A. Picaud, S.M. Wu, R. Marc, and F. Werblin Postsynaptic response kinetics are controlled by a glutamate transporter at cone photoreceptors J. Neurophysiol. 79 1998 190 196
94. C.C. Garner, S. Kindler, and E.D. Gundelfinger Molecular determinants of presynaptic active zones Curr. Opin. Neurobiol. 10 2000 321 327
95. 2+ sensor for transmitter release at a central synapse Cell 79 1994 717 727
96. S.H. Gerber, J. Garcia, J. Rizo, and T.C. Sudhof An unusual C(2)-domain in the active-zone protein piccolo: implications for Ca(2+) regulation of neurotransmitter release EMBO J. 20 2001 1605 1619
97. H.M. Gerschenfeld, and M. Piccolino Sustained feedback effects of L-horizontal cells on turtle cones Proc. R. Soc. Lond. B Biol. Sci. 206 1980 465 480
98. 2+ influx and efflux Neuron 13 1994 1109 1117
99. E. Glowatzki, and P.A. Fuchs Transmitter release at the hair cell ribbon synapse Nat. Neurosci. 5 2002 147 154
100. B.F. Godley, and R.J. Wurtman Release of endogenous dopamine from the superfused rabbit retina in vitro: effect of light stimulation Brain Res. 452 1988 393 395
101. A. Gomis, J. Burrone, and L. Lagnado Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells J. Neurosci. 19 1999 6309 6317
102. A. Gosbell, I. Favilla, and P. Jablonski The effects of insulin on the electroretinogram of bovine retina in vitro Curr. Eye Res. 15 1996 1132 1137
103. G.B. Grant, and F.S. Werblin A glutamate-elicited chloride current with transporter-like properties in rod photoreceptors of the tiger salamander Vis. Neurosci. 13 1996 135 144
104. M. Gratzl, G. Dahl, J.T. Russell, and N.A. Thorn Fusion of neurohypophyseal membranes in vitro Biochim. Biophys. Acta 470 1977 45 57
105. E.G. Gray Microtubules in synapses of the retina J. Neurocytol. 5 1976 361 370
106. P. Greengard, F. Benfenati, and F. Valtorta Synapsin I, an actin-binding protein regulating synaptic vesicle traffic in the nerve terminal Adv. Second Messenger Phosphoprotein Res. 29 1994 31 45
107. 2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function Nat. Neurosci. 7 2004 1079 1087
108. S. Haverkamp, and W.D. Eldred Localization of nNOS in photoreceptor, bipolar and horizontal cells in turtle and rat retinas Neuroreport 9 1998 2231 2235
109. S. Haverkamp, and H. Wassle Characterization of an amacrine cell type of the mammalian retina immunoreactive for vesicular glutamate transporter 3 J. Comp. Neurol. 468 2004 251 263
110. R. Heidelberger Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse J. Gen. Physiol. 111 1998 225 241
111. R. Heidelberger Electrophysiological approaches to the study of neuronal exocytosis and synaptic vesicle dynamics Rev. Physiol. Biochem. Pharmacol. 143 2001 1 80
112. R. Heidelberger, C. Heinemann, E. Neher, and G. Matthews Calcium dependence of the rate of exocytosis in a synaptic terminal Nature 371 1994 513 515
113. R. Heidelberger, and G. Matthews Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons J. Physiol. (Lond.) 447 1992 235 256
114. R. Heidelberger, P. Sterling, and G. Matthews Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles J. Neurophysiol. 88 2002 98 106
115. R. Heidelberger, M.M. Wang, and D.M. Sherry Differential distribution of synaptotagmin immunoreactivity among synapses in the goldfish, salamander, and mouse retina Vis. Neurosci. 20 2003 37 49
116. D. Henderson, T.A. Doerr, J. Gottesman, and R.F. Miller Calcium channel immunoreactivity in the salamander retina Neuroreport 17 2001 1493 1499
117. 2+ channels Neuron 34 2002 411 423
118. M.H. Higgs, and P.D. Lukasiewicz Activation of group II metabotropic glutamate receptors inhibits glutamate release from salamander retinal photoreceptors Vis. Neurosci. 19 2002 275 281
119. B. Hille Ionic Channels of Excitable Membranes 1993 Sinauer Associates Sunderland, MA
120. 2+ channels J. Gen. Physiol. 122 2003 657 671
121. H. Hirasawa, R. Shiells, and M. Yamada Analysis of spontaneous EPSCs in retinal horizontal cells of the carp Neurosci. Res. 40 2001 75 86
122. H. Hirasawa, R. Shiells, and M. Yamada A metabotropic glutamate receptor regulates transmitter release from cone presynaptic terminals in carp retinal slices J. Gen. Physiol. 119 2002 55 68
123. N. Hirokawa, and R. Takemura Kinesin superfamily proteins and their various functions and dynamics Exp. Cell Res. 301 2004 50 59
124. M. Holt, A. Cooke, M.M. Wu, and L. Lagnado Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells J. Neurosci. 23 2003 1329 1339
125. M. Holt, A. Cooke, A. Neef, and L. Lagnado High mobility of vesicles supports continuous exocytosis at a ribbon synapse Curr. Biol. 14 2004 173 183
126. J. Howard Molecular motors: structural adaptations to cellular functions Nature 389 1997 61 567
127. T. Ichinose, C.R. Shields, and P.D. Lukasiewicz Sodium channels in transient retinal bipolar cells enhance visual responses in ganglion cells J. Neurosci. 25 2005 1856 1865
128. U. Janssen-Bienhold, K. Schultz, A. Gellhaus, P. Schmidt, J. Ammermuller, and R. Weiler Identification and localization of connexin26 within the photoreceptor-horizontal cell synaptic complex Vis. Neurosci. 18 2001 169 178
129. C.L. Jelsema, and J. Axelrod Stimulation of phospholipase A2 activity in bovine rod outer segments by the beta gamma subunits of transducin and its inhibition by the alpha subunit Proc. Natl. Acad. Sci. USA 84 1987 3623 3627
130. H. Jiang, A. Lyubarsky, R. Dodd, N. Vardi, E. Pugh, D. Baylor, M.I. Simon, and D. Wu Phospholipase C β4 is involved in modulating the visual response in mice Proc. Natl. Acad. Sci. USA 93 1996 14598 14601
131. C. Job, and L. Lagnado Calcium and protein kinase C regulate the actin cytoskeleton in the synaptic terminal of retinal bipolar cells J. Cell Biol. 143 1998 1661 1672
132. J. Johnson, H. Wong, J.H. Walsh, and N.C. Brecha Expression of the somatostatin subtype 2a receptor in the rabbit retina J. Comp. Neurol. 393 1998 93 101
133. J. Johnson, V. Wu, H. Wong, J.H. Walsh, and N.C. Brecha Somatostatin receptor subtype 2a expression in the rat retina Neuroscience 94 1999 675 683
134. J. Johnson, M.L. Caravelli, and N.C. Brecha Somatostatin inhibits calcium influx into rat rod bipolar cell axonal terminals Vis. Neurosci. 18 2001 101 108
135. J. Johnson, N. Tian, M.S. Caywood, R.J. Reimer, R.H. Edwards, and D.R. Copenhagen Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate J. Neurosci. 23 2003 518 529
136. J. Johnson, D.M. Sherry, X. Liu, R.T. Fremeau Jr., R.P. Seal, R.H. Edwards, and D.R. Copenhagen Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retina J. Comp. Neurol. 477 2004 386 398
137. S. Johnson, S. Halford, A.G. Morris, R.J. Patel, S.E. Wilkie, A.J. Hardcastle, A.T. Moore, K. Zhang, and D.M. Hunt Genomic organisation and alternative splicing of human RIM1, a gene implicated in autosomal dominant cone-rod dystrophy (CORD7) Genomics 81 2003 304 314
138. 2+ dependence of exocytosis during development of mouse inner hair cells J. Physiol. (Lond.) 563 2004 177 191
139. 2+ channels by conditioning voltage and divalent ions Biophys. J. 83 2002 2587 2594
140. H. Jung, and C. Reme Light-evoked arachidonic acid release in the retina: illuminance/duration dependence and the effects of quinacrine, mellitin and lithium. Light-evoked arachidonic acid release Graefes Arch. Clin. Exp. Ophthalmol. 232 1994 167 175
141. M. Kamermans, and I. Fahrenfort Ephaptic interactions within a chemical synapse: hemichannel-mediated ephaptic inhibition in the retina Curr. Opin. Neurobiol. 14 2004 531 541
142. M. Kamermans, and H. Spekreijse The feedback pathway from horizontal cells to cones. A mini review with a look ahead Vision Res. 39 1999 2449 2468
143. M. Kamermans, I. Fahrenfort, K. Schultz, U. Janssen-Bienhold, T. Sjoerdsma, and R. Weiler Hemichannel-mediated inhibition in the outer retina Science 292 2001 1178 1180
144. W. Kamphuis, and H. Hendriksen Expression patterns of voltage-dependent calcium channel alpha 1 subunits (alpha 1A-alpha 1E) mRNA in rat retina Brain Res. Mol. Brain Res. 55 1998 209 220
145. A. Kaneko, and M. Tachibana Effects of γ-aminobutyric acid on isolated cone photoreceptors of the turtle retina J. Physiol. (Lond.) 373 1986 443 461
146. Y. Kang, X. Huang, E.A. Pasyk, J. Ji, G.G. Holz, M.B. Wheeler, R.G. Tsushima, and H.Y. Gaisano Syntaxin-3 and syntaxin-1A inhibit L-type calcium channel activity, insulin biosynthesis and exocytosis in beta-cell lines Diabetologia 45 2002 231 241
147. M. Kano, O. Garaschuk, A. Verkhratsky, and A. Konnerth Ryanodine receptor - mediated intracellular calcium release in rat cerebellar Purkinje neurons J. Physiol. (Lond.) 487 1995 1 16
148. F. Kawai Characterization of spontaneous excitatory synaptic currents in newt retinal bipolar cells Neurosci. Lett. 271 1999 49 52
149. D. Khimich, R. Nouvian, R. Pujol, S. tomDieck, A. Egner, E.D. Gundelfinger, and T. Moser Hair cell synaptic ribbons are essential for synchronous auditory signaling Nature 434 2005 889 894
150. H.G. Kim, and R.F. Miller Rods and cones activate different excitatory amino acid receptors on the mudpuppy retinal horizontal cell Brain Res. 538 1991 141 146
151. H.G. Kim, and R.F. Miller Properties of synaptic transmission from photoreceptors to bipolar cells in the mudpuppy retina J. Neurophysiol. 69 1993 352 360
152. K.S. Kits, and H.D. Mansvelder Regulation of exocytosis in neuroendocrine cells: spatial organization of channels and vesicles, stimulus-secretion coupling, calcium buffers and modulation Brain Res. Brain Res. Rev. 33 2000 78 94
153. K.S. Kits, T.A. de Vlieger, B.W. Kooi, and H.D. Mansvelder Diffusion barriers limit the effect of mobile calcium buffers on exocytosis of large dense cored vesicles Biophys. J. 76 1999 1693 1705
154. S.J. Kleene, and R.C. Gesteland Calcium-activated chloride conductance in frog olfactory cilia J. Neurosci. 11 1991 3624 3629
155. U. Klockner, and G. Isenberg Calcium channel current of vascular smooth muscle cells: extracellular protons modulate gating and single channel conductance J. Gen. Physiol. 103 1994 665 678
156. A. Kobayashi, T. Higashide, D. Hamasaki, S. Kubota, H. Sakuma, W. An, T. Fujimaki, M.J. McLaren, R.G. Weleber, and G. Inana HRG4 (UNC119) mutation found in cone-rod dystrophy causes retinal degeneration in a transgenic model Invest. Ophthalmol. Vis. Sci. 41 2000 3268 3277
157. H. Kolb Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells Philos. Trans. R. Soc. Lond. B 258 1970 261 283
158. S. Kondo, R. Sato-Yoshitake, Y. Noda, H. Aizawa, T. Nakata, Y. Matsuura, and N. Hirokawa KIF3A is a new microtubule-based anterograde motor in the nerve axon J. Cell Biol. 125 1994 1095 1107
159. 2+-dependent inactivation J. Neurosci. 23 2003 6041 6049
160. P. Koulen, and J.H. Brandstatter Pre- and Postsynaptic Sites of Action of mGluR8a in the mammalian retina Invest. Ophthalmol. Vis. Sci. 43 2002 1933 1940
161. P. Koulen, R. Kuhn, H. Wassle, and J.H. Brandstatter Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor Proc. Natl. Acad. Sci. USA 96 1999 9909 9914
162. P. Koulen, J. Liu, E. Nixon, and C. Madry Interaction between mGluR8 and calcium channels in photoreceptors is sensitive to pertussis toxin and occurs via G protein betagamma subunit signaling Invest. Ophthalmol. Vis. Sci. 46 2005 287 291
163. D.E. Kurenny, X. Liu, J. Hart, F. Mahmud, W.H. Baldridge, and S. Barnes Reciprocal modulation of calcium dynamics at rod and cone photoreceptor synapses by nitric oxide J. Neurophysiol. 92 2004 477 483
164. D.A. Kraaij, H. Spekreijse, and M. Kamermans The nature of surround-induced depolarizing responses in goldfish cones J. Gen. Physiol. 115 2000 3 16
165. D.S. Krafte, and R.S. Kass Hydrogen ion modulation of Ca channel current in cardiac ventricular cells. Evidence for multiple mechanisms J. Gen. Physiol. 91 1988 641 657
166. M. Kreft, D. Krizaj, S. Grilc, and R. Zorec Properties of exocytotic response in vertebrate photoreceptors J. Neurophysiol. 90 2003 218 225
167. D. Krizaj, and D.R. Copenhagen Calcium regulation in photoreceptors Front. Biosci. 7 2002 2023 2044
168. D. Krizaj, R. Gabriel, W.G. Owen, and P. Witkovsky Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina J. Comp. Neurol. 398 1998 529 538
169. D. Krizaj, J.X. Bao, Y. Schmitz, P. Witkovsky, and D.R. Copenhagen Caffeine-sensitive calcium stores regulate synaptic transmission from retinal rod photoreceptors J. Neurosci. 19 1999 7249 7261
170. D. Krizaj, F.A. Lai, and D.R. Copenhagen Ryanodine stores and calcium regulation in the inner segments of salamander rods and cones J. Physiol. (Lond.) 547 2003 761 774
171. D. Krizaj, X. Liu, and D.R. Copenhagen Expression of calcium transporters in the retina of the tiger salamander (Ambystoma tigrinum) J. Comp. Neurol. 475 2004 463 480
172. D.E. Kurenny, G.A. Thurlow, R.W. Turner, L.L. Moroz, K.A. Sharkey, and S. Barnes Nitric oxide synthase in tiger salamander retina J. Comp. Neurol. 361 1995 525 536
173. D.E. Kurenny, L.L. Moroz, R.W. Turner, K.A. Sharkey, and S. Barnes Modulation of ion channels in rod photoreceptors by nitric oxide Neuron 13 1994 315 324
174. R. Kurtz, A.K. Warzecha, and M. Egelhaaf Transfer of visual motion information via graded synapses operates linearly in the natural activity range J. Neurosci. 21 2001 6957 6966
175. A. Kvanta, S. Seregard, S. Sejersen, B. Kull, and B.B. Fredholm Localization of adenosine receptor messenger RNAs in the rat eye Exp. Eye Res. 65 1997 595 602
176. L. Lagnado, A. Gomis, and C. Job Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells Neuron 17 1996 957 967
177. H.P. Larsson, S.A. Picaud, F.S. Werblin, and H. Lecar Noise analysis of the glutamate-activated current in photoreceptors Biophys. J. 70 1996 733 742
178. A. Lasansky Cell junctions at the outer synaptic layer of the retina Invest. Ophthalmol. 11 1972 265 275
179. A. Lasansky Organization of the outer synaptic layer in the retina of the larval tiger salamander Philos. Trans. R. Soc. B. 265 1973 471 489
180. A. Lasansky Contacts between receptors and electrophysiologically identified neurones in the retina of the larval tiger salamander J. Physiol. (Lond.) 285 1978 531 542
181. E.M. Lasater, and P. Witkovsky The calcium current of turtle cone photoreceptor axon terminals Neurosci. Res. Suppl. 15 1991 S165 S173
182. D.R. Lazzell, R. Belizaire, P. Thakur, D.M. Sherry, and R. Janz SV2B regulates synaptotagmin 1 by direct interaction J. Biol. Chem. 279 2004 52124 52131
183. D. Lenzi, and H. von Gersdorff Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines BioEssays 23 2001 831 840
184. D. Lenzi, J.W. Runyeon, J. Crum, M.H. Ellisman, and W.M. Roberts Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography J. Neurosci. 19 1999 119 132
185. R.R. Llinas, M. Sugimori, K.A. Moran, J.E. Moreira, and M. Fukuda Vesicular reuptake inhibition by a synaptotagmin I C2B domain antibody at the squid giant synapse Proc. Natl. Acad. Sci. USA 101 2004 17855 17860
186. A. Llobet, V. Beaumont, and L. Lagnado Real-time measurement of exocytosis and endocytosis using interference of light Neuron 40 2003 075 86
187. A. Llobet, A. Cooke, and L. Lagnado Exocytosis at the ribbon synapse of retinal bipolar cells studied in patches of presynaptic membrane J. Neurosci. 23 2003 2706 2714
188. Q. Lu, A. Straiker, Q. Lu, and G. Maguire Expression of CB2 cannabinoid receptor mRNA in adult rat retina Vis. Neurosci. 17 2000 91 95
189. K. Luby-Phelps Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area Int. Rev. Cytol. 192 2000 189 221
190. J.W. Mandell, E. Townes-Anderson, A.J. Czernik, R. Cameron, P. Greengard, and P. DeCamilli Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses Neuron 5 1990 19 33
191. J.W. Mandell, A.J. Czernik, P. de Camilli, P. Greengard, and E. Townes-Anderson Differential expression of synapsins I and II among rat retinal synapses J. Neurosci. 12 1992 1736 1749
192. H.D. Mansvelder, and K.S. Kits The relation of exocytosis and rapid endocytosis to calcium entry evoked by short repetitive depolarizing pulses in rat melanotropic cells J. Neurosci. 18 1998 81 92
193. H.D. Mansvelder, and K.S. Kits All classes of calcium channel couple with equal efficiency to exocytosis in rat melanotropes, inducing linear stimulus-secretion coupling J. Physiol. (Lond.) 526 2000 327 339
194. B.R. Maple, F.S. Werblin, and S.M. Wu Miniature excitatory postsynaptic currents in bipolar cells of the tiger salamander retina Vision Res. 34 1994 2357 2362
195. R.E. Marc, W.K. Stell, D. Bok, and D.M. Lam GABA-ergic pathways in the goldfish retina J. Comp. Neurol. 182 1978 221 244
196. A.V. Maricq, and J.I. Korenbrot Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors Neuron 1 1988 503 515
197. M. Matsumura, S. Okinami, and M. Ohkuma Synaptic vesicle exocytosis in goldfish photoreceptor cells Albrecht Von Graefes Arch. Klin. Exp. Ophthalmol. 215 1981 159 170
198. G. Matthews Synaptic exocytosis and endocytosis: capacitance measurements Curr. Opin. Neurobiol. 6 1996 358 364
199. G. Matthews Cycling the synapse: scenic versus direct route for vesicles Neuron 44 2004 223 226
200. A.K. McAllister, and C.F. Stevens Nonsaturation of AMPA and NMDA receptors at hippocampal synapses Proc. Natl. Acad. Sci. USA 97 2000 6173 6178
201. P. McCaffery, J. Mey, and U.C. Drager Light-mediated retinoic acid production Proc. Natl. Acad. Sci. USA 93 1996 12570 12574
202. T.F. McDonald, S. Pelzer, W. Trautwein, and D.J. Pelzer Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells Physiol. Rev. 74 1994 365 507
203. J.E. McRory, J. Hamid, C.J. Doering, E. Garcia, R. Parker, K. Hamming, L. Chen, M. Hildebrand, A.M. Beedle, L. Feldcamp, G.W. Zamponi, and T.P. Snutch The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution J. Neurosci. 24 2004 1707 1718
204. S. Mennerick, and G. Matthews Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons Neuron 17 1996 1241 1249
205. S. Mennerick, and C.F. Zorumski Presynaptic influence on the time course of fast excitatory synaptic currents in cultured hippocampal cells J. Neurosci. 15 1995 3178 3192
206. N. Minami, K. Berglund, T. Sakaba, H. Kohmoto, and M. Tachibana Potentiation of transmitter release by protein kinase C in goldfish retinal bipolar cells J. Physiol. (Lond.) 512 1998 219 225
207. I.M. Mintz, B.L. Sabatini, and W.G. Regehr Calcium control of transmitter release at a cerebellar synapse Neuron 15 1995 675 688
208. L.N. Moller, C.E. Stidsen, B. Hartmann, and J.J. Holst Somatostatin receptors Biochim. Biophys. Acta 1616 2003 1 84
209. C.W. Morgans Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina Eur. J. Neurosci. 11 1999 2989 2993
210. C.W. Morgans Presynaptic proteins of ribbon synapses in the retina Microsc. Res. Tech. 50 2000 141 150
211. C.W. Morgans Localization of the α1F calcium channel subunit in the rat retina Invest. Ophthalmol. Vis. Sci. 42 2001 2414 2418
212. C.W. Morgans, J.H. Brandstatter, J. Kellerman, H. Betz, and H. Wassle A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina J. Neurosci. 16 1996 6713 6721
213. C.W. Morgans, O. El Far, A. Berntson, H. Wassle, and W.R. Taylor Calcium extrusion from mammalian photoreceptor terminals J. Neurosci. 18 1998 2467 2474
214. A. Moriondo, B. Pelucchi, and G. Rispoli Calcium-activated potassium current clamps the dark potential of vertebrate rods Eur. J. Neurosci. 14 2001 19 26
215. Z. Muresan, and J.C. Besharse D2-like dopamine receptors in amphibian retina: localization with fluorescent ligands J. Comp. Neurol. 331 1993 149 160
216. V. Muresan, E. Bendala-Tufanisco, B.A. Hollander, and J.C. Besharse KIF3C and KIF3A form a novel neuronal heteromeric kinesin that associates with membrane vesicles Mol. Biol. Cell. 9 1998 637 652
217. V. Muresan, A. Lyass, and B.J. Schnapp The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors J. Neurosci. 19 1999 1027 1037
218. G.J. Murphy, L.L. Glickfeld, Z. Balsen, and J.S. Isaacson Sensory neuron signaling to the brain: properties of transmitter release from olfactory nerve terminals J. Neurosci. 24 2004 3023 3030
219. M. Nachman-Clewner, R. St Jules, and E. Townes-Anderson L-type calcium channels in the photoreceptor ribbon synapse: localization and role in plasticity J. Comp. Neurol. 415 1999 1 16
220. A.R. Nagy, and P. Witkovsky A freeze-fracture study of synaptogenesis in the distal retina of larval Xenopus J. Neurocytol. 10 1981 897 919
221. S. Naito, and T. Ueda Characterization of glutamate uptake into synaptic vesicles J. Neurochem. 44 1985 99 109
222. K.I. Naka, M.A. Itoh, and R.L. Chappell Dynamics of turtle cones J. Gen. Physiol. 89 1987 321 337
223. S. Nawy, and C.E. Jahr Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells Nature 346 1990 269 271
224. 2+ microdomains: new tools for understanding their roles in neurotransmitter release Neuron 20 1998 389 399
225. G. Neves, and L. Lagnado The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells J. Physiol. (Lond.) 515 1999 181 202
226. P.M. O'Bryan Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina J. Physiol. (Lond.) 235 1973 207 223
227. T.J. O'Dell, and B.E. Alger Single calcium channels in rat and guinea-pig hippocampal neurons J. Physiol. (Lond.) 436 1991 739 767
228. H. Ohnishi, S. Yamamori, K. Ono, K. Aoyagi, S. Kondo, and M. Takahashi A src family tyrosine kinase inhibits neurotransmitter release from neuronal cells Proc. Natl. Acad. Sci. USA 98 2001 10930 10935
229. T.S. Otis, Y.C. Wu, and L.O. Trussell Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites J. Neurosci. 16 1996 1634 1644
230. G. Owen Ionic conductances in rod photoreceptors Annu. Rev. Physiol. 49 1987 743 764
231. R. Paes de Carvalho, K.M. Braas, S.H. Snyder, and R. Adler Analysis of adenosine immunoreactivity, uptake, and release in purified cultures of developing chick embryo retinal neurons and photoreceptors J. Neurochem. 55 1990 1603 1611
232. 1 receptors, uptake sites and endogenous adenosine in chick retina Dev. Brain Res. 70 1992 87 95
233. C. Paillart, J. Li, G. Matthews, and P. Sterling Endocytosis and vesicle recycling at a ribbon synapse J. Neurosci. 23 2003 4092 4099
234. K. Palczewski, A.S. Polans, W. Baehr, and J.B. Ames Ca(2+)-binding proteins in the retina: structure, function, and the etiology of human visual diseases Bioessays 22 2000 337 350
235. Z.H. Pan, H.J. Hu, P. Perring, and R. Andrade T-type Ca(2+) channels mediate neurotransmitter release in retinal bipolar cells Neuron 32 2001 89 98
236. J.J. Pang, F. Gao, and S.M. Wu Stratum-by-stratum projection of light response attributes by retinal bipolar cells of Ambystoma J. Physiol. (Lond.) 558 2004 249 262
237. T.D. Parsons, and P. Sterling Synaptic ribbon. Conveyor belt or safety belt? Neuron 37 2003 379 382
238. Y.W. Peng, A.H. Sharp, S.H. Snyder, and K.W. Yau Localization of the inositol 1,4,5-trisphosphate receptor in synaptic terminals in the vertebrate retina Neuron 6 1991 525 531
239. S.A. Picaud, H.P. Larsson, G.B. Grant, H. Lecar, and F.S. Werblin Glutamate-gated chloride channel with glutamate-transporter-like properties in cone photoreceptors of the tiger salamander J. Neurophysiol. 74 1995 1760 1771
240. M. Piccolino, A.L. Byzov, D.E. Kurenny, A. Pignatelli, F. Sappia, M. Wilkinson, and S. Barnes Low-calcium-induced enhancement of chemical synaptic transmission from photoreceptors to horizontal cells in the vertebrate retina Proc. Natl. Acad. Sci. USA 93 1996 2302 2306
241. M. Piccolino, V. Vellani, L.A. Rakotobe, A. Pignatelli, S. Barnes, and P. Mc Naughton Manipulation of synaptic sign and strength with divalent cations in the vertebrate retina: pushing the limits of tonic, chemical neurotransmission Eur. J. Neurosci. 11 1999 4134 4138
242. R.L. Pierantoni, and G.D. McCann A quantitative study on synaptic ribbons in the photoreceptors of turtle and frog A. Borsellino L. Cervetto Photoreceptors 1981 Plenum Press New York 255 283
243. A. Porcella, C. Maxia, G.L. Gessa, and L. Pani The human eye expresses high levels of CB1 cannabinoid receptor mRNA and protein Eur. J. Neurosci. 12 2000 1123 1127
244. D.V. Pow, N.L. Barnett, and P. Penfold Are neuronal transporters relevant in retinal glutamate homeostasis? Neurochem. Int. 37 2000 191 198
245. H. Qian, L. Li, R.L. Chappell, and H. Ripps GABA receptors of bipolar cells from the skate retina: actions of zinc on GABA-mediated membrane currents J. Neurophysiol. 78 1997 2402 2412
246. K. Rabl, and W.B. Thoreson Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions Eur. J. Neurosci. 16 2002 2070 2077
247. K. Rabl, E.J. Bryson, and W.B. Thoreson Activation of glutamate transporters in rods inhibits presynaptic calcium currents Vis. Neurosci. 20 2003 557 566
248. V. Ralevic, and G. Burnstock Receptors for purines and pyrimidines Pharmacol. Rev. 50 1998 413 492
249. R. Rao-Mirotznik, A.B. Harkins, G. Buchsbaum, and P. Sterling Mammalian rod terminal: architecture of a binary synapse Neuron 14 1995 561 569
250. R. Rao-Mirotznik, G. Buchsbaum, and P. Sterling Transmitter concentration at a three-dimensional synapse J. Neurophysiol. 80 1998 3163 3172
251. E. Raviola, and N.B. Gilula Intramembrane organization of specialized contacts in the outer plexiform layer of the retina J. Cell Biol. 75 1975 192 222
252. R. Rea, J. Li, A. Dharia, E.S. Levitan, P. Sterling, and R.H. Kramer Streamlined synaptic vesicle cycle in cone photoreceptor terminals Neuron 4 2004 755 766
253. S. Redenti, and R.L. Chappell Zinc chelation enhances the sensitivity of the ERG b-wave in dark-adapted skate retina Biol. Bull. 205 2003 213 214
254. S. Redman Quantal analysis of synaptic potentials in neurons of the central nervous system Physiol. Rev. 70 1990 165 198
255. J.J. Reinboth, M. Clausen, and C.E. Reme Light elicits the release of docosahexaenoic acid from membrane phospholipids in the rat retina in vitro Exp. Eye Res. 63 1996 277 284
256. C.E. Reiter, and T.W. Gardner Functions of insulin and insulin receptor signaling in retina possible implications for diabetic retinopathy Prog. Retin. Eye Res. 22 2003 545 562
257. C. Ribelayga, and S.C. Mangel A circadian clock and light/dark adaptation differentially regulate adenosine in the mammalian retina J. Neurosci. 25 2005 215 222
258. F. Rieke, and E.A. Schwartz A cGMP-gated current can control exocytosis at cone synapses Neuron 13 1994 863 873
259. F. Rieke, and E.A. Schwartz Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse J. Physiol. (Lond.) 493 1996 1 8
260. 3-sensitive channels that are sensed by neighboring mitochondria Science 262 1993 744 747
261. 2+ channels in hair cells from bullfrog saccule J. Physiol. (Lond.) 538 2002 729 745
262. 2+ channels in hair cells Biophys. J. 84 2003 3457 3469
263. F.J. Rosenstein, and R.L. Chappell Endogenous zinc as a retinal neuromodulator: evidence from the skate (Raja erinacea) Neurosci. Lett. 345 2003 81 84
264. B. Roska, L. Gaal, and F.S. Werblin Voltage-dependent uptake is a major determinant of glutamate concentration at the cone synapse: an analytical study J. Neurophysiol. 80 1998 1951 1960
265. N.C. Rouze, and E.A. Schwartz Continuous and transient vesicle cycling at a ribbon synapse J. Neurosci. 18 1998 8614 8624
266. S.J. Royle, and L. Lagnado Endocytosis at the synaptic terminal J. Physiol. (Lond.) 553 2003 345 355
267. B. Rudy Diversity and ubiquity of K channels Neuroscience 25 1988 729 750
268. T. Sakaba, M. Tachibana, K. Matsui, and N. Minami Two components of transmitter release in retinal bipolar cells: exocytosis and mobilization of synaptic vesicles Neurosci. Res. 27 1997 357 370
269. T. Sakaba, R. Schneggenburger, and E. Neher Estimation of quantal parameters at the calyx of Held synapse Neurosci. Res. 44 2002 343 356
270. H.M. Sakai, and K. Naka Signal transmission in the catfish retina. V. Sensitivity and circuit J. Neurophysiol. 58 1987 1329 1350
271. M. Sarantis, and P. Mobbs The spatial relationship between Muller cell processes and the photoreceptor output synapse Brain Res. 584 1992 299 304
272. A. Savchenko, S. Barnes, and R.H. Kramer Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide Nature 390 1997 694 698
273. S.F. Schaeffer, E. Raviola, and J.E. Heuser Membrane specializations in the outer plexiform layer of the turtle retina J. Comp. Neurol. 204 1982 253 267
274. F. Schmitz, A. Konigstorfer, and T.C. Sudhof RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function Neuron 28 2000 857 872
275. Y. Schmitz, and P. Witkovsky Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel Neuroscience 78 1997 1209 1216
276. D.M. Schneeweis, and J.L. Schnapf Photovoltage of rods and cones in the macaque retina Science 268 1995 1053 1056
277. + Am. J. Physiol. 257 1989 C153 C157
278. E.A. Schwartz Synaptic transmission in amphibian retinae during conditions unfavourable for calcium entry into presynaptic terminals J. Physiol. (Lond.) 376 1986 411 428
279. Z.H. Sheng, J. Rettig, M. Takahashi, and W.A. Catterall Identification of a syntaxin-binding site on N-type calcium channels Neuron 13 1994 1303 1313
280. Z.H. Sheng, C.T. Yokoyama, and W.A. Catterall Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery J. Bioenerg. Biomembr. 30 1998 335 345
281. D.M. Sherry, H. Yang, and K.M. Standifer Vesicle-associated membrane protein isoforms in the tiger salamander retina J. Comp. Neurol. 431 2001 424 436
282. D.M. Sherry, M.M. Wang, J. Bates, and L.J. Frishman Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits J. Comp. Neurol. 465 2003 480 498
283. D.M. Sherry, M.M. Wang, and L.J. Frishman Differential distribution of vesicle associated membrane protein isoforms in the mouse retina Mol. Vis. 9 2003 673 688
284. 2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse J. Neurosci. 23 2003 10923 10933
285. J.H. Singer, L. Lassova, N. Vardi, and J.S. Diamond Coordinated multivesicular release at a mammalian ribbon synapse Nat. Neurosci. 7 2004 826 833
286. 2+ channels in mouse cerebellar granule cells J. Physiol. (Lond.) 439 1991 301 323
287. A.P. Somlyo, and B. Walz Elemental distribution in Rana pipiens retinal rods: quantitative electron probe analysis J. Physiol. (Lond.) 358 1985 183 195
288. E.F. Stanley Presynaptic calcium channels and the depletion of synaptic cleft calcium ions J. Neurophysiol. 83 2000 477 482
289. E.F. Stanley Syntaxin I modulation of presynaptic calcium channel inactivation revealed by botulinum toxin C1 Eur. J. Neurosci. 17 2003 1303 1305
290. E.F. Stanley, and R.R. Mirotznik Cleavage of syntaxin prevents G-protein regulation of presynaptic calcium channels Nature 385 1997 340 343
291. S.L. Stella, and W.B. Thoreson Differential modulation of rod and cone calcium currents in tiger salamander retina by D2 dopamine receptors and camp Eur. J. Neurosci. 12 2000 3537 3548
292. S.L. Stella, E.J. Bryson, and W.B. Thoreson Insulin inhibits voltage-dependent calcium influx into rod photoreceptors Neuroreport 12 2001 947 951
293. 2 adenosine receptors inhibit calcium influx through L-type calcium channels in rod photoreceptors of the tiger salamander retina J. Neurophysiol. 87 2002 333 350
294. S.L. Stella, E.J. Bryson, L. Cadetti, and W.B. Thoreson Endogenous adenosine reduces glutamatergic output from rods through activation of A2-like adenosine receptors J. Neurophysiol. 90 2003 165 174
295. P. Sterling, and G. Matthews Structure and function of ribbon synapses Trends Neurosci. 28 2005 20 29
296. A. Straiker, and J.M. Sullivan Cannabinoid receptor activation differentially modulates ion channels in photoreceptors of the tiger salamander J. Neurophysiol. 89 2003 2647 2654
297. A. Straiker, N. Stella, D. Piomelli, K. Mackie, H.J. Karten, and G. Maguire Cannabinoid CB1 receptors and ligands in vertebrate retina: localization and function of an endogenous signaling system Proc. Natl. Acad. Sci. USA 96 1999 14565 14570
298. K.M. Studholme, and S. Yazulla 3H-adenosine uptake selectively labels rod horizontal cells in goldfish retina Vis. Neurosci. 14 1997 207 212
299. T.C. Sudhof Synaptotagmins: why so many? J. Biol. Chem. 277 2002 7629 7632
300. T.C. Sudhof The synaptic vesicle cycle Annu. Rev. Neurosci. 27 2004 509 547
301. S. Sugita, O.H. Shin, W. Han, Y. Lao, and T.C. Sudhof Synaptotagmins form a hierarchy of exocytotic Ca(2+) sensors with distinct Ca(2+) affinities EMBO J. 21 2002 270 280
302. M. Takahashi, M. Itakura, and M. Kataoka New aspects of neurotransmitter release and exocytosis: regulation of neurotransmitter release by phosphorylation J. Pharmacol. Sci. 93 2003 41 45
303. S. Takamori, J.S. Rhee, C. Rosenmund, and R. Jahn Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons Nature 407 2000 189 194
304. W.R. Taylor, and C. Morgans Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri Vis. Neurosci. 15 1998 541 552
305. G. Tesoriere, G. Calvaruso, R. Vento, M. Giuliano, M. Lauricella, and M. Carabillo Insulin synthesis in chick embryo retinas during development Neurochem. Res. 19 1994 821 825
306. K. Thermos Functional mapping of somatostatin receptors in the retina: a review Vision Res. 43 2003 1805 1815
307. W.B. Thoreson, and E.J. Bryson Chloride equilibrium potential in salamander cones BMC Neurosci. 5 2005 53
308. W.B. Thoreson, and D.A. Burkhardt Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination Vis. Neurosci. 5 1990 571 583
309. W.B. Thoreson, and D.A. Burkhardt Ionic influences on the prolonged depolarization of turtle cones in situ J. Neurophysiol. 65 1991 96 110
310. W.B. Thoreson, and R.F. Miller Removal of extracellular chloride suppresses transmitter release from photoreceptor terminals in the mudpuppy retina J. Gen. Physiol. 107 1996 631 642
311. W.B. Thoreson, and S.L. Stella Jr. Anion modulation of calcium current voltage dependence and amplitude in salamander rods Biochim. Biophys. Acta 1464 2000 142 150
312. W.B. Thoreson, and P. Witkovsky Glutamate receptors and circuits in the vertebrate retina Prog. Retin. Eye Res. 18 1999 765 810
313. 2+ currents and synaptic transmission in amphibian photoreceptors J. Neurophysiol. 77 1997 2175 2190
314. W.B. Thoreson, R. Nitzan, and R.F. Miller Chloride efflux inhibits single calcium channel open probability in vertebrate photoreceptors: chloride imaging and cell-attached patch-clamp recordings Vis. Neurosci. 17 2000 197 206
315. 2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina Vis. Neurosci. 19 2002 235 247
316. W.B. Thoreson, E.J. Bryson, and K. Rabl Reciprocal interactions between calcium and chloride in rod photoreceptors J. Neurophysiol. 90 2003 1747 1753
317. W.B. Thoreson, D. Tranchina, and P. Witkovsky Kinetics of synaptic transfer from rods and cones to horizontal cells in the salamander retina Neuroscience 122 2003 785 798
318. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse Neuron 42 2004 595 605
319. S. tom Dieck, W.D. Altrock, M.M. Kessels, B. Qualmann, H. Regus, D. Brauner, A. Fejtova, O. Bracko, E.D. Gundelfinger, and J.H. Brandstätter Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex J. Cell Biol. 168 2005 825 836
320. K. Tornqvist, R. Uddman, F. Sundler, and B. Ehinger Somatostatin and VIP neurons in the retina of different species Histochemistry 76 1982 137 152
321. E. Townes-Anderson, P.R. MacLeish, and E. Raviola Rod cells dissociated from mature salamander retina: ultrastructure and uptake of horseradish peroxidase J. Cell Biol. 100 1985 175 188
322. J.-I. Toyoda Membrane resistance changes underlying the bipolar cell response in the carp retina Vision Res. 13 1973 283 294
323. D. Tranchina, J. Gordon, R. Shapley, and J. Toyoda Linear information processing in the retina: a study of horizontal cell responses Proc. Natl. Acad. Sci. USA 78 1981 6540 6542
324. E.B. Trexler, W. Li, and S.C. Massey Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses J. Neurophysiol. 93 2005 1476 1485
325. B. Ullrich, and T.C. Sudhof Distribution of synaptic markers in the retina: implications for synaptic vesicle traffic in ribbon synapses J. Physiol. (Paris) 88 1994 249 257
326. O. Umino, and K. Watanabe Decline of blocking effect of cobalt ions on transmission from photoreceptors to horizontal cells during its prolonged application Neurosci. Lett. 82 1987 291 296
327. J. Usukura, and E. Yamada Ultrastructure of the synaptic ribbons in photoreceptor cells of Rana catesbeiana revealed by freeze-etching and freeze-substitution Cell Tissue Res. 247 1987 483 488
328. H.A. Van Epps, M. Hayashi, L. Lucast, G.W. Stearns, J.B. Hurley, P. deCamilli, and S.E. Brockerhoff The zebrafish nrc mutant revela s arole for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring J. Neurosci. 24 2004 8641 8650
329. M.C. Van Rossum, and R.G. Smith Noise removal at the rod synapse of mammalian retina Vis. Neurosci. 15 1998 809 821
330. 2+ current in salamander photoreceptors by polyunsaturated fatty acids and retinoids J. Physiol. (Lond.) 529 2000 333 344
331. V. Venkataraman, T. Duda, N. Vardi, K.W. Koch, and R.K. Sharma Calcium-modulated guanylate cyclase transduction machinery in the photoreceptor - bipolar synaptic region Biochemistry 42 2003 5640 5648
332. J. Verweij, M. Kamermans, and H. Spekreijse Horizontal cells feed back to cones by shifting the cone calcium-current activation range Vision Res. 36 1996 3943 3953
333. J.P. Vessey, M.R. Lalonde, H.A. Mizan, N.C. Welch, M.E. Kelly, and S. Barnes Carbenoxolone inhibition of voltage-gated Ca channels and synaptic transmission in the retina J. Neurophysiol. 92 2004 1252 1256
334. J. Vigh, and P. Witkovsky Sub-millimolar cobalt selectively inhibits the receptive field surround of retinal neurons Vis. Neurosci. 16 1999 159 168
335. L. Vollrath, and I. Spiwoks-Becker Plasticity of retinal ribbon synapses Microsc. Res. Tech. 35 1996 472 487
336. H. von Gersdorff, and G. Matthews Inhibition of endocytosis by elevated internal calcium in a synaptic terminal Nature 370 1994 652 655
337. H. von Gersdorff, and G. Matthews Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons J. Neurosci. 16 1996 115 122
338. H. von Gersdorff, E. Vardi, G. Matthews, and P. Sterling Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released Neuron 16 1996 1221 1227
339. H. von Gersdorff, T. Sakaba, K. Berglund, and M. Tachibana Submillisecond kinetics of glutamate release from a sensory synapse Neuron 21 1998 1177 1188
340. K. Von Kriegstein, and F. Schmitz The expression pattern and assembly profile of synaptic membrane proteins in ribbon synapses of the developing mouse retina Cell Tissue Res. 311 2003 159 173
341. K. Von Kriegstein, F. Schmitz, E. Link, and T.C. Sudhof Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses Eur. J. Neurosci. 11 1999 1335 1348
342. 2+ currents in rat neurohypophysial terminals J. Neurophysiol. 70 1993 1617 1628
343. Y. Wang, M. Okamoto, F. Schmitz, K. Hofmann, and T.C. Sudhof Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion Nature 388 1997 593 598
344. T.L. Wang, P. Sterling, and N. Vardi Localization of type I inositol 1,4,5-triphosphate receptor in the outer segments of mammalian cones J. Neurosci. 19 1999 4221 4228
345. M.M. Wang, R. Janz, R. Belizaire, L.J. Frishman, and D.M. Sherry Differential distribution and developmental expression of synaptic vesicle protein 2 isoforms in the mouse retina J. Comp. Neurol. 460 2003 106 122
346. R. Weiler, W.H. Baldridge, S.C. Mangel, and J.E. Dowling Modulation of endogenous dopamine release in the fish retina by light and prolonged darkness Vis. Neurosci. 14 1997 351 356
347. M.F. Wilkinson, and S. Barnes The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors J. Gen. Physiol. 197 1996 621 630
348. P. Witkovsky Dopamine and retinal function Doc. Ophthalmol. 108 2004 17 40
349. P. Witkovsky, S. Stone, and J.C. Besharse Dopamine modifies the balance of rod and cone inputs to horizontal cells of the Xenopus retina Brain Res. 449 1988 332 336
350. P. Witkovsky, S. Stone, and D. Tranchina Photoreceptor to horizontal cell synaptic transfer in the Xenopus retina: modulation by dopamine ligands and a circuit model for interactions of rod and cone inputs J. Neurophysiol. 62 1989 864 881
351. P. Witkovsky, C. Nicholson, M.E. Rice, K. Bohmaker, and E. Meller Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis Proc. Natl. Acad. Sci. USA 90 1993 5667 5671
352. P. Witkovsky, Y. Schmitz, A. Akopian, D. Krizaj, and D. Tranchina Gain of rod to horizontal cell synaptic transfer: relation to glutamate release and a dihydropyridine-sensitive calcium current J. Neurosci. 17 1997 7297 7306
353. P. Witkovsky, W.B. Thoreson, and D. Tranchina Transmission at the photoreceptor synapse Prog. Brain Res. 131 2001 145 159
354. S.M. Wu Synaptic transmission from rods to bipolar cells in the tiger salamander retina Proc. Natl. Acad. Sci. USA 82 1985 3944 3947
355. S.M. Wu Synaptic transmission from rods to horizontal cells in dark-adapted tiger salamander retina Vision Res. 28 1988 1 8
356. S.M. Wu, X. Qiao, J.L. Noebels, and X.L. Yang Localization and modulatory actions of zinc in vertebrate retina Vision Res. 33 1993 2611 2626
357. L.G. Wu, R.E. Westenbroek, J.G. Borst, W.A. Catterall, and B. Sakmann Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses J. Neurosci. 19 1999 726 736
358. J.W. Xu, and M.M. Slaughter Large conductance calcium activated potassium channels (BK) enhance synaptic transmission at the photoreceptor synapse ARVO Abstract 1142 2004
359. T. Yagi, and P.R. MacLeish Ionic conductances of monkey solitary cone inner segments J. Neurophysiol. 71 1994 656 665
360. H. Yamazaki, T. Nakata, Y. Okada, and N. Hirokawa KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport J. Cell Biol. 130 1995 1387 1399
361. S. Yazulla, K.M. Studholme, H.H. McIntosh, and D.G. Deutsch Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina J. Comp. Neurol. 415 1999 80 90
362. D. Zenisek, J.A. Steyer, and W. Almers Transport, capture and exocytosis of single synaptic vesicles at active zones Nature 406 2000 849 854
363. D. Zenisek, V. Davila, L. Wan, and W. Almers Imaging calcium entry sites and ribbon structures in two presynaptic cells J. Neurosci. 23 2003 2538 2548
364. D. Zenisek, N.K. Horst, C. Merrifield, P. Sterling, and G. Matthews Visualizing synaptic ribbons in the living cell J. Neurosci. 24 2004 9752 9759
365. D.Q. Zhang, C. Ribelayga, S.C. Mangel, and D.G. McMahon Suppression by zinc of AMPA receptor-mediated synaptic transmission in the retina J. Neurophysiol. 88 2002 1245 1251
366. Y. Zhang, and W.O. Hancock The two motor domains of KIF3A/B coordinate for processive motility and move at different speeds Biophys. J. 87 2004 1795 1804